Review
Plant sphingolipids: structural diversity, biosynthesis, first genes and functions

https://doi.org/10.1016/S1388-1981(03)00033-7Get rights and content

Abstract

In mammals and Saccharomyces cerevisiae, sphingolipids have been a subject of intensive research triggered by the interest in their structural diversity and in mammalian pathophysiology as well as in the availability of yeast mutants and suppressor strains. More recently, sphingolipids have attracted additional interest, because they are emerging as an important class of messenger molecules linked to many different cellular functions. In plants, sphingolipids show structural features differing from those found in animals and fungi, and much less is known about their biosynthesis and function. This review focuses on the sphingolipid modifications found in plants and on recent advances in the functional characterization of genes gaining new insight into plant sphingolipid biosynthesis. Recent studies indicate that plant sphingolipids may be also involved in signal transduction, membrane stability, host–pathogen interactions and stress responses.

Introduction

Sphingolipids are ubiquitous membrane components in eukaryotic cells and in a few bacteria [1], [2]. Their chemical structure differs from the more commonly known glycerolipids in having a ceramide backbone, which consists of a fatty acid attached to a long-chain amino alcohol. Recent interest is focussing on the role of sphingolipids in serving as intra- and intercellular second messengers regulating cell growth, differentiation, apoptosis, and pathogenic defense [3], [4]. Compared to the tremendous research on bioactive sphingolipids in mammalian systems and Saccharomyces cerevisiae published during the last two decades, there is a paucity of studies using plant systems. Studies on sphingolipid metabolism in plants have focused on demonstrating and characterizing the in vitro activities of enzymatic steps in major pathways [5]. The success in elucidating additional aspects of their metabolism and in recognizing first functions are mainly due to the fact that genes controlling crucial steps in the biosynthesis of sphingolipids have been identified only recently from plants and some other phyla.

These notable and recent advancements in the knowledge of plant sphingolipid biosynthesis and function will be summarized here together with an indication of remaining gaps and possible future research directions. In many studies, S. cerevisiae served as a model organism to study sphingolipid metabolism and seems to become the first eukaryotic organism in which all sphingolipid metabolic genes are identified. However, this statement does not apply to the biosynthesis and functions of the structural diverse plant sphingolipids. Indeed, divergencies in the biosynthetic pathway of plants lead to cerebrosides and glycosyl inositol phosphorylceramides (GIPC) with a preference for Δ8-unsaturated long-chain bases (LCB) [6], [7], [8], [9], [10], [11], [12] not present in baker's yeast. Despite or just because of the exceptional absence of cerebrosides and unsaturated LCB in yeast, this organism has been successfully used for the functional identification of heterologously expressed genes involved in plant sphingolipid synthesis. In this way, genes encoding enzymes modifying the ceramide core have been recently identified from a variety of different phyla including plants [13], [14], [15], [16], [17]. Sequence comparisons shed new light on evolutionary relationships of some of these proteins [16], [18]. An extrapolation of the success with S. cerevisiae as a model suggests that the generation of plant mutants affecting sphingolipid metabolism will promote the elucidation of sphingolipid functions. Targeted gene disruption by homologous recombination established for the moss Physcomitrella patens [19], [20], RNAi antisense inactivation [21], [22] and the identification of transposon-tagged Arabidopsis thaliana mutants [23], [24] will provide unprecedented opportunities to identify and characterize new functions for plant sphingolipids.

In the first part, this review will give an overview of the structures of sphingolipids found in plants, thereby placing emphasis on seemingly minor structural modifications compared to other phyla which may have unexpected relevance on sphingolipid functions. Based on the recent progress in understanding the molecular biology of sphingolipid biosynthesis, we will then develop a current picture of this pathway in plants. The knowledge of the functions of sphingolipids and their precursors in plants has just started to advance [25], [26], [27]. We will summarize recent data from this field trying to focus on features of plant sphingolipids not covered by previous reviews [5], [25], [26], [27], [28], [29].

Section snippets

Structural diversity of plant sphingolipids

Sphingolipids are generated by the addition of a polar head group to ceramides which in turn are composed of a LCB (2-amino-1,3-dihydroxyalkane) carrying a N-acylated fatty acid of 14–26 carbon atoms. Complex sphingolipids, such as cerebrosides and GIPC (phytoglycolipids) are formed by the addition of various glycosyl residues and other polar phosphate-containing headgroups to the ceramide. Depending on the source, this basic ceramide structure can be modified by differences in chain length,

Characterization of plant genes for sphingolipid biosynthesis

In the following, recent progress in the cloning and identification of genes involved in sphingolipid biosynthesis of plants will be discussed with emphasis on the synthesis of the characteristic unsaturated LCB. A scheme for the proposed pathway of sphingolipid synthesis in plants is shown in Fig. 3. Many of the proteins involved still need further biochemical characterization, in particular their subcellular localization in the plant cell. For an easier comparison, the gene names from S.

First functions of sphingolipids in plants

There is still little information on the functions of sphingolipids in plants. Their roles in cell signalling, membrane stability, stress response, pathogenesis and apoptosis have been recently reviewed [25], [26], [27]. However, there are interesting roles emerging which will be shortly summarized.

Conclusions

Since the complete genomic sequence of A. thaliana is available and sequencing projects of other plant genomes are currently in progress, putative candidate genes coding for nearly every enzyme involved in plant sphingolipid metabolism may be identified in databases. After annotation, genes can be functionally characterized by heterologous expression in suitable eukaryotic model organisms such as yeast and S. pombe, or by complementation of orthologous mutants. Subsequently, further enzymatic

Acknowledgements

We thank Dr. Dirk Warnecke for fruitful discussions. The work in the authors' laboratory was supported by the BASF AG, by the Deutsche Forschungsgemeinschaft, by the Sonderforschungsbereich 470 and by the BMBF project NAPUS 2000.

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